Archives of Physical Medicine and Rehabilitation
Volume 89, Issue 7 , Pages 1221-1229 , July 2008

The Effect of Exercise Training in Improving Motor Performance and Corticomotor Excitability in People With Early Parkinson's Disease

Presented in part to the Society for Neuroscience, October 17, 2006, Atlanta, GA; American Physical Therapy Association Combined Sections, February 1–5, 2006, San Diego, CA; the World Parkinson Congress, February 22–26, 2006, Washington, DC; and the National Parkinson Foundation Collaboration for Care Leadership Conference, October 20–22, 2005, San Francisco, CA.

  • Beth E. Fisher, PhD

      Affiliations

    • Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA
    • Division of Neurology, University of Southern California, Los Angeles, CA
    • Corresponding Author InformationCorrespondence to Beth Fisher, PhD, Div of Biokinesiology and Physical Therapy, University of Southern California, 1540 E Alcazar St, CHP 155, Los Angeles, CA 90089-9006
    • ,
  • Allan D. Wu, MD

      Affiliations

    • Department of Neurology, David Geffen School of Medicine, UCLA, Los Angeles, CA.
    • ,
  • George J. Salem, PhD

      Affiliations

    • Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA
    • ,
  • Jooeun Song, MS

      Affiliations

    • Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA
    • ,
  • Chien-Ho (Janice) Lin, PhD

      Affiliations

    • Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA
    • ,
  • Jeanine Yip, DPT

      Affiliations

    • Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA
    • ,
  • Steven Cen, PhD

      Affiliations

    • Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA
    • ,
  • James Gordon, EdD

      Affiliations

    • Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA
    • ,
  • Michael Jakowec, PhD

      Affiliations

    • Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA
    • Division of Neurology, University of Southern California, Los Angeles, CA
    • ,
  • Giselle Petzinger, MD

      Affiliations

    • Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA
    • Division of Neurology, University of Southern California, Los Angeles, CA

References 

  1. Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci. 1996;16:785–807
  2. Fisher BE, Petzinger GM, Nixon K, et al. Exercise-induced behavioral recovery and neuroplasticity in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse basal ganglia. J Neurosci Res. 2004;77:378–390
  3. Adkins DL, Boychuk J, Remple MS, Kleim JA. Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J Appl Physiol. 2006;101:1776–1782
  4. Miyai I, Fujimoto Y, Ueda Y, et al. Treadmill training with body weight support: its effect on Parkinson's disease. Arch Phys Med Rehabil. 2000;81:849–852
  5. Miyai I, Fujimoto Y, Yamamoto H, et al. Long-term effect of body weight-supported treadmill training in Parkinson's disease: a randomized controlled trial. Arch Phys Med Rehabil. 2002;83:1370–1373
  6. Toole T, Maitland CG, Warren E, Hubmann MF, Panton L. The effects of loading and unloading treadmill walking on balance, gait, fall risk, and daily function in Parkinsonism. NeuroRehabilitation. 2005;2:307–322
  7. Cakit BD, Saracoglu M, Genc H, Erdem HR, Inan L. The effects of incremental speed-dependent treadmill training on postural instability and fear of falling in Parkinson's disease. Clin Rehabil. 2007;21:698–705
  8. Herman T, Giladi N, Gruendlinger L, Hausdorff JM. Six weeks of intensive treadmill training improves gait and quality of life in patients with Parkinson's disease: a pilot study. Arch Phys Med Rehabil. 2007;88:1154–1158
  9. Pohl M, Rockstroh G, Ruckriem S, Mrass G, Mehrholz J. Immediate effects of speed-dependent treadmill training on gait parameters in early Parkinson's disease. Arch Phys Med Rehabil. 2003;84:1760–1766
  10. Schenkman M, Hall D, Kumar R, Kohrt WM. Endurance exercise training to improve economy of movement of people with Parkinson disease: three case reports. Phys Ther. 2008;88:63–76
  11. Nutt JG, Wooten GF. Diagnosis and initial management of Parkinson's disease. N Engl J Med. 2005;353:1021–1027
  12. Clarke CE. Parkinson's disease. BMJ. 2007;335:441–445
  13. Frenkel-Toledo S, Giladi N, Peretz C, Herman T, Gruendlinger L, Hausdorff J. Effect of gait speed on gait rhythmicity in Parkinson's disease: variability of stride time and swing time respond differently. J Neuro Eng Rehabil. 2005;2:1–7
  14. Cantello R, Gianelli M, Bettucci D, Civardi C, De Angelis MS, Mutani R. Parkinson's disease rigidity: magnetic motor evoked potentials in a small hand muscle. Neurology. 1991;41:1449–1456
  15. Valls-Sole J, Pascual-Leone A, Brasil-Neto JP, Cammarota A, McShane L, Hallett M. Abnormal facilitation of the response to transcranial magnetic stimulation in patients with Parkinson's disease. Neurology. 1994;44:735–741
  16. Cantello R, Gianelli M, Civardi C, Mutani R. Magnetic brain stimulation: the silent period after the motor evoked potential. Neurology. 1992;42:1951–1959
  17. Dioszeghy P, Hidasi E, Mechler F. Study of central motor functions using magnetic stimulation in Parkinson's disease. Electromyogr Clin Neurophysiol. 1999;39:101–105
  18. Cantello R, Tarletti R, Civardi C. Transcranial magnetic stimulation and Parkinson's disease. Brain Res Brain Res Rev. 2002;38:309–327
  19. Strafella AP, Valzania F, Nassetti SA, et al. Effects of chronic levodopa and pergolide treatment on cortical excitability in patients with Parkinson's disease: a transcranial magnetic stimulation study. Clin Neurophysiol. 2000;111:1198–1202
  20. Young MS, Triggs WJ, Bowers D, Greer M, Friedman WA. Stereotactic pallidotomy lengthens the transcranial magnetic cortical stimulation silent period in Parkinson's disease. Neurology. 1997;49:1278–1283
  21. Dauper J, Peschel T, Schrader C, et al. Effects of subthalamic nucleus (STN) stimulation on motor cortex excitability. Neurology. 2002;59:700–706
  22. Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology. 1967;17:427–442
  23. Kieburtz K. Designing neuroprotection trials in Parkinson's disease. Ann Neurol. 2003;53:S100–S109
  24. Kieburtz K. Issues in neuroprotection clinical trials in Parkinson's disease. Neurology. 2006;66:S50–S57
  25. Folstein MF, Folstein SE, McHugh PR. “Mini-mental state” (A practical method for grading the cognitive state of patients for the clinician). J Psychiatr Res. 1975;12:189–198
  26. Taylor AH, Cable NT, Faulkner G, Hillsdon M, Narici M, Van Der Bij AK. Physical activity and older adults: a review of health benefits and the effectiveness of interventions. J Sports Sci. 2004;22:703–725
  27. Gibbons RJ, Balady GJ, Bricker JT, et al. American College of Cardiology/American Heart Association Task Force on Practice Guidelines Committee to Update the 1997 Exercise Testing Guidelines ACC/AHA 2002 guideline update for exercise testing: summary article (A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee to Update the 1997 Exercise Testing Guidelines)). [published erratum in: J Am Coll Cardiol 2006;48:17]. J Am Coll Cardiol. 2002;40:1531–1540
  28. Deane KH, Ellis-Hill C, Jones D, et al. Systematic review of paramedical therapies for Parkinson's disease. Mov Disord. 2002;17:984–991
  29. Deane KH, Jones D, Ellis-Hill C, Clarke CE, Playford ED, Ben-Shlomo Y. A comparison of physiotherapy techniques for patients with Parkinson's disease. Cochrane Database Syst Rev. 2001;(1):CD002815
  30. Ainsworth BE, Haskell WL, Leon AS, et al. Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sports Exerc. 1993;25:71–80
  31. Fahn S, Elton RL, Fahn S, Marsden CD, Calne DB, Goldstein M. Unified Parkinson's Disease Rating Scale: recent developments in Parkinson's disease. In: Florham Park: Macmillan Healthcare Information; 1987;p. 153–163
  32. Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. Electroencephalogr Clin Neurophysiol. 1998;108:1–16
  33. Anand S, Hotson J. Transcranial magnetic stimulation: neurophysiological applications and safety. Brain Cogn. 2002;50:366–386
  34. Brasil-Neto JP, Cohen LG, Panizza M, Nilsson J, Roth BJ, Hallett M. Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J Clin Neurophysiol. 1992;9:132–136
  35. Koski L, Schrader LM, Wu AD, Stern JM. Normative data on changes in transcranial magnetic stimulation measures over a ten hour period. Clin Neurophysiol. 2005;116:2099–2109
  36. Daskalakis ZJ, Molnar GF, Christensen BK, Sailer A, Fitzgerald PB, Chen R. An automated method to determine the transcranial magnetic stimulation-induced contralateral silent period. Clin Neurophysiol. 2003;114:938–944
  37. Devanne H, Lavoie BA, Capaday C. Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res. 1997;114:329–338
  38. Kimiskidis VK, Papagiannopoulos S, Sotirakoglou K, Kazis DA, Kazis A, Mills KR. Silent period to transcranial magnetic stimulation: construction and properties of stimulus–response curves in healthy volunteers. Exp Brain Res. 2005;V163:21–31
  39. Lopopolo RB, Greco M, Sullivan D, Craik RL, Mangione KK. Effect of therapeutic exercise on gait speed in community-dwelling elderly people: a meta-analysis. Phys Ther. 2006;86:520–540
  40. Kerrigan DC, Todd MK, Della Croce U, Lipsitz LA, Collins JJ. Biomechanical gait alterations independent of speed in the healthy elderly: evidence for specific limiting impairments. Arch Phys Med Rehabil. 1998;79:317–322
  41. Sofuwa O, Nieuwboer A, Desloovere K, Willems AM, Chavret F, Jonkers I. Quantitative gait analysis in Parkinson's disease: comparison with a healthy control group. Arch Phys Med Rehabil. 2005;86:1007–1013
  42. Ferrarin M, Rizzone M, Bergamasco B, et al. Effects of bilateral subthalamic stimulation on gait kinematics and kinetics in Parkinson's disease. Exp Brain Res. 2005;160:517–527
  43. Baltadjieva R, Giladi N, Gruendlinger L, Peretz C, Hausdorff JM. Marked alterations in the gait timing and rhythmicity of patients with de novo Parkinson's disease. Eur J Neurosci. 2006;24:1815–1820
  44. Lefaucheur JP. Motor cortex dysfunction revealed by cortical excitability studies in Parkinson's disease: influence of antiparkinsonian treatment and cortical stimulation. Clin Neurophysiol. 2005;116:244–253
  45. Priori A, Berardelli A, Inghilleri M, Accornero N, Manfredi M. Motor cortical inhibition and the dopaminergic system (Pharmacological changes in the silent period after transcranial brain stimulation in normal subjects, patients with Parkinson's disease and drug-induced parkinsonism). Brain. 1994;117(Pt 2):317–323
  46. Nakashima K, Wang Y, Shimoda M, Sakuma K, Takahashi K. Shortened silent period produced by magnetic cortical stimulation in patients with Parkinson's disease. J Neurol Sci. 1995;130:209–214
  47. Ridding MC, Inzelberg R, Rothwell JC. Changes in excitability of motor cortical circuitry in patients with Parkinson's disease. Ann Neurol. 1995;37:181–188
  48. Manfredi L, Garavaglia P, Beretta S, Pellegrini G. Increased cortical inhibition induced by apomorphine in patients with Parkinson's disease. Neurophysiol Clin. 1998;28:31–38
  49. Ziemann U, Bruns D, Paulus W. Enhancement of human motor cortex inhibition by the dopamine receptor agonist pergolide: evidence from transcranial magnetic stimulation. Neurosci Lett. 1996;208:187–190
  50. Brasil-Neto JP, Cammarota A, Valls-Sole J, Pascual-Leone A, Hallett M, Cohen LG. Role of intracortical mechanisms in the late part of the silent period to transcranial stimulation of the human motor cortex. Acta Neurol Scand. 1995;92:383–386
  51. Galvan A, Wichmann T. GABAergic circuits in the basal ganglia and movement disorders. Progress Brain Res. 2007;160:287–312
  52. Cotman CW, Berchtold NC. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 2002;25:295–301
  53. Cotman CW, Berchtold NC, Christie LA. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci. 2007;30:464–472
  54. Cotman CW, Engesser-Cesar C. Exercise enhances and protects brain function. Exerc Sport Sci Rev. 2002;30(2):75–79
  55. Swanwick CC, Murthy NR, Kapur J. Activity-dependent scaling of GABAergic synapse strength is regulated by brain-derived neurotrophic factor. Mole Cell Neurosci. 2006;31:481–492
  56. Bardoni R, Ghirri A, Salio C, Prandini M, Merighi A. BDNF-mediated modulation of GABA and glycine release in dorsal horn lamina II from postnatal rats. Dev Neurobiol. 2007;67:960–975
  57. Norton JA, Gorassini MA. Changes in cortically related intermuscular coherence accompanying improvements in locomotor skills in incomplete spinal cord injury. J Neurophysiol. 2006;95:2580–2589
  58. Thomas SL, Gorassini MA. Increases in corticospinal tract function by treadmill training after incomplete spinal cord injury. J Neurophysiol. 2005;94:2844–2855
  59. Forrester LW, Hanley DF, Macko RF. Effects of treadmill exercise on transcranial magnetic stimulation-induced excitability to quadriceps after stroke. Arch Phys Med Rehabil. 2006;87:229–234
  60. Petzinger GM, Walsh JP, Akopian G, et al. Effects of treadmill exercise on dopaminergic transmission in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse model of basal ganglia injury. J Neurosci. 2007;27:5291–5300

 Supported by the Kinetics Foundation and National Institute of Neurological Disorders and Stroke (grant no. K23-NS045764).

 No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the author(s) or on any organization with which the author(s) is/are associated.

 Reprints are not available from the author.

 Published online June 5, 2008 at www.archives-pmr.org.

PII: S0003-9993(08)00235-9

doi: 10.1016/j.apmr.2008.01.013

Archives of Physical Medicine and Rehabilitation
Volume 89, Issue 7 , Pages 1221-1229 , July 2008

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